EFFECTS OF THE PRECIPITATION REGIMEN AND SPATIAL SCALE ON THE INVERTEBRATE COMMUNITIES AND ECOSYSTEM PROCESSES IN
PHYTOTELMATA
A Thesis Presented to The Biological Science Faculty
by
Fabiola Ospina Bautista
In partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Science
Universidad de los Andes
2 ABSTRACT
Understanding the factors that drive community structure and ecosystem processes are a
relevant goal in ecology. One factor is environmental heterogeneity that alters
communities through changes in habitat and available resource for species; however, it
is unclear if those effects can change according to the spatial scale. Another factor is
climate change, which affects community composition and ecosystem functionality
through the loss of particular predator species; although, it is unknown if rainfall
variability can alter the community and energy and nutrient flux in temporal
ecosystems, such as ponds or phytotelmata.
We used the community within two phytotelmata, bromeliads and tree holes, as an
ecological model system in order to assess effect of spatial scale and hydrological
regime on communities and ecosystem processes. First, we studied the invertebrate
community associated to Guzmania multiflora (André) André ex Mez. (Bromeliaceae)
and their biological traits. We assessed the relation between biological traits and habitat
complexity and resource availability. We found that habitat complexity not only alters
the taxonomical diversity of invertebrates in bromeliads, but also their functional
diversity through changes in the abundance and richness of biological traits. In this
regard, biological traits provide an approach to ecosystem processes and invertebrate
adaptations to environmental conditions. Second, we investigated the effects of spatial scale dependence of habitat and detritus on community and decomposition. We found
that species turnover of invertebrates associated with tree holes depended on a spatial
scale and that there was a scale-dependent effect of habitat and litter on the community
and litter decomposition. Third, we assessed the relationship between the amount and
3 the magnitude of precipitation rather than rainfall frequency affected invertebrate
communities, decomposition, and primary productivity. Finally, we analyzed the energy
and nitrogen flux in a bromeliad invertebrate food web and its interaction with the loss
of an intraguild predator. We found that the interaction between shifts in the amount of
precipitation and the presence/absence of the predator altered the energy and nitrogen
4 TABLE OF CONTENTS
ABSTRACT ... 2
LIST OF TABLES ... 6
LIST OF FIGURES ... 8
ACKNOWLEDGMENTS ... 12
OBJETIVES ... 14
GENERAL OBJETIVES ... 14
SPECIFIC OBJETIVES ... 14
CHAPTER 1. INTRODUCTION ... 15
1.1. REFERENCES ... 21
CHAPTER 2. INVERTEBRATE COMMUNITY ASSOCIATED TO GUZMANIA MULTIFLORA (BROMELIACEA) IN CLOUD MOUNTAIN: HABITAT COMPLEXITY AND AVAILABLE ENERGY AFFECTS BIOLOGICAL TRAITS. ... 35
2.1. ABSTRACT ... 35
2.2. INTRODUCTION ... 35
2.3. METHODS ... 38
2.3.1. Study Area ... 38
2.3.2. Methods ... 38
2.3.3. Statistical analysis ... 39
2.4. RESULTS ... 40
2.5. DISCUSION ... 41
2.5.1. Taxonomical diversity ... 41
2.5.2. Biological traits diversity ... 43
2.6. REFERENCES ... 46
3. CHAPTER 3: SCALE DEPENDENCE OF HABITAT AND LITTER TYPE EFFECTS ON TREE HOLES COMMUNITIES... 67
3.1. ABSTRACT ... 67
3.2. INTRODUCTION ... 67
3.3. METHODS ... 70
3.3.1. Model system ... 70
3.3.2. Experiment 1. Micro scale (Canopy vs. understory)... 71
3.3.3. Experiment 2. Meso scale (Forest vs. plantation) ... 71
3.3.3. Experiment 3. Macro scale (Elevation gradient) ... 72
3.3.4. Data analysis ... 74
3.4. RESULTS ... 75
3.4.1. Micro scale (Canopy vs. Understory) ... 75
3.4.2. Meso scale (Plantation vs Forest) ... 76
3.4.3. Macro scale (Low, Middle, High elevation ... 77
3.5. DISCUSSION ... 78
3.6. REFERENCES ... 80
4. CHAPTER 4: SCALE DEPENDENCE OF HABITAT AND RESOURCE HETEROGENEITY EFFECTS ON DECOMPOSITION IN TREE HOLES ... 91
4.1. ABSTRACT ... 91
5
4.3. METHODS ... 9594
4.3.1. Micro scale: Canopy vs. understory ... 95
4.3.2. Meso scale: Forest vs. plantation ... 96
4.3.3. Macro scale: Elevation gradient ... 97
4.3.4. Statistical analysis ... 98
4.4. RESULTS ... 98
4.5. DISCUSSION ... 100
4.6. REFERENCES ... 104
CHAPTER 5: PRECIPITATION REGIMEN AFFECTS THE COMMUNITY AND ECOSYSTEM PROCESSES OF BROMELIADS ... 116
5.1. ABSTRACT ... 116
5.2. INTRODUCTION ... 116
5.3. METHODS ... 120
5.3.1. Study area ... 120
5.3.2. Experiment ... 120
5.3.3. Statistical analysis ... 124
5.4. RESULTS ... 126
5.4.1. Environmental conditions ... 126
5.4.2. Invertebrate community ... 126
5.4.3. Bacteria community ... 128
5.4.4. Ecosystem processes ... 129
5.5. DISCUSSION ... 129
5.5.1. Environmental variables ... 130
5.5.2. Invertebrates Community ... 131
5.5.3. Bacteria Community ... 132
5.5.4. Ecosystem processes ... 133
5.6. REFERENCES ... 136
6. CHAPTER 6: HYDROLOGICAL REGIMEN EFFECT ON NITROGEN AND ENERGY FLUX IN A FOOD WEB ... 165
6.1. ABSTRACT ... 165
6.2. INTRODUCTION ... 166
6.3. METHODS ... 169
6.3.1. Study Area ... 169
6.3.2. Statistical analyses ... 172
6.4. RESULTS ... 173
6.4.1. Environmental variables ... 173
6.4.2. Survival of insects ... 173
6.4.3. Flux of energy ... 174
6.4.4. Flux of Nitrogen ... 175
6.5. DISCUSSION ... 175
6.6. REFERENCES ... 180
6 LIST OF TABLES
Table 2.1. Abundance of invertebrates associated to Guzmania multiflora Habitat: T:
Terrestrial, A: Aquatic; Stage: Ad: Adult, L: Larvae, P: Pupa. ……….………57
Table 2.2. Relation of Leaf number and litter weight with abundance and richness for categories of biological traits of invertebrate into Guzmania multiflora……….61
Table 3.1. Generalized linear models of abundance and number of species associated to
tree hole at different habitat. The variable statistical significant is
highlighted………...87
Table 3.2. Betadiversity Mean and Standard Deviation of the litter treatment in the
elevation gradient experiment ………88
Table 4.1. Effects of response variable on water temperature and pH of tree holes at the
micro, meso, and macro scale. The variable statistical significant is highlighted.
.……….………113
Table 5.1. Effects of mean amount of rainfall per day and dispersion parameter on
7 Table 5.2. Invertebrate abundance found in the experiment. Habitat T=Terrestrial,
Aq=Aquatic; Stage: A=Adult, I=Immature ……….……….…150
Table 5.3. Generalized linear models for abundance and number of species of macro
invertebrate community with Gaussian family. MU= rainfall per day; K: dispersion
parameter……… 153
Table 5.4. ANOVA Betadiversity Disimilarity Index for abundance and
presence/ausence of macroinvertebrate. MU= rainfall per day; K: dispersion
parameter...……….……… 156
Table 5.5. Effects of mean amount of rainfall per day, dispersion parameter, depth of
water, temperature daily, hydroperiod and days without water on ecosystem process.
GAM; MU= mean amount of rainfall per day; K=dispersion parameter. Highlight
values are significant……….……….………...157
Table 6.1. Generalized linear models assessing the influence of precipitation and trophic
structure treatments on the biomass, abundance of d15N (‰), nitrogen concentration (N
%), and survival for each trophic level in the
8 LIST OF FIGURES
Figure 2.1. Number of species per invertebrate order found in Guzmania multiflora………..…64
Figure 2.2. Relation between leaf number and abundance (A) and Number of species
(B) of macroinvertebrates associated to Guzmania multiflora ………..…65
Figure 2.3. Abundance and richness of biological traits of macroinvertebrates associated
to Guzmania multiflora A. Abundance of habitat; B. Abundance of stage; C. Abundance
of dispersion; D. Richness Functional groups; E. Abundance of Functional groups.………..………...66
Figure 3.1. Bray Curtis beta diversity according to habitats in each scale. A. Microscale,
B Meso scale, C. Macro scale ……….………89
Figure 3.2. Percentage of variation of community in each spatial scale according to
variable measure in each scale………..………...90
Figure 4.1. Percentage of variation of litter decomposition at each spatial scale
according to habitat, litter, interaction, and not explained ………….………...………114
9 Figure 4.2. Percentage of remaining litter for each litter and habitat type. A. Micro
scale; B. Meso scale; C. Macro scale Non mix A: Alnus acuminata, Non mix B: Piper
imperiale, Non mix C: Croton magdalenensis, Mix A: A. acuminata and P. imperiale,
Mix B: A. acuminata and C. magdelenensis, Mix C: P. imperiale and C. magdelenensis,
Mix D: A. acuminata, C. magdelenensis, and P.
imperial………..115
Figure 5.1. Precipitation records (mm) of study area for each month from 1997 to 2012 ……..………..159
Figure 5.2. Variation in environmental variable through shift in the amount of rainfall
and dispersion parameter. A. Hydroperiod; B. Days without water; C. Mean of depth of
water; D. Mean of daily temperature………....….160
Figure 5.3. Abundance of invertebrate according to MU (mean rainfall amount) and K
(dispersion parameter). A. Abundace total of invertebrate; B. Abundance of aquatic
invertebrate ………..161
Figure 5.4. Number of invertebrate species according to MU (mean rainfall amount) and
K (dispersion parameter). A. Number of species total; B. Number of species terrestrial;
C. Number of species aquatic………162
Figure 5.5. Shift in the decomposition process according to mean rainfall amount, depth
10 Variation of FPOM with water depth mean; C. Variation of detritus loss percentage
with hydroperiod. D. Variation of detritus loss percentage with depth mean……….…..163
Figure 5.6. Shift in the Chlorophyll-A and turbidity according to mean rainfall amount
and hydroperiod. A. Variation of Chlorophyll-A with rainfall amount (MU); B.
Variation of turbidity with mean rainfall amount (MU)
………164
Figure 6.1. Trophic structure with species and number of individuals of each trophic
group utilize in the experiment. A. Trophic structure with presence of Oreiallagma
oreas (predator). B. Trophic structure without O. oreas.
……….……….191
Figure 6.2. Shift in biomass of each trophic level into food web according to
precipitation regimen and predator presence. A. Fine particle organic matter mass; B.
Biomass of litter; C. Shift in the filter feeder (Culicidae) biomass; D. Shift in the
detritivores (Scirtes sp.) biomass; E. Shift in the predator (O. oreas) biomass.
Precipitation treatments correspond to 0.1X, 1X and 3x of the rainfall mean. Predator
treatment correspond presence or absence of predator (O. oreas)……….………192
Figure 6.3. Difference in Δδ13C-values (Delta δ13Cfinal−initial) (‰), for each trophic
11 C (‰) of litter leaf; B. Δδ 13 C(‰) of detritivores (Scirtes sp.); C. Δδ 13 C(‰) of filter
feeder (Culex sp.); D. Δδ 13 C(‰) of predator (O. oreas). Precipitation treatments
correspond to 0.1X, 1X and 3x of the rainfall mean. Predator treatment correspond
presence or absence of predator (O. oreas)
………..………..…....193
Figure 6.4. Shift in the Nitrogen percentage of each trophic level into food web
according to precipitation regimen and predator presence. A. Delta of nitrogen
percentage of litter leaf; B. Nitrogen percentage of Fine particle organic matter mass;
C. Delta of nitrogen percentage of filter feeder (Culex sp.); D. Delta of nitrogen
percentage of detritivores (Scirtes sp.); E. Delta of nitrogen percentage of thepredator
(O. oreas). Precipitation treatments correspond to 0.1X, 1X and 3x of the rainfall mean.
Predator treatment correspond presence or absence of predator (O.
oreas)………...….…194
Figure 6.5. Difference of abundance of Δδ15N (‰), for each trophic level into food web
according to precipitation regimen and predator presence. A. Δδ 15N (‰) of litter leaf;
B. δ15N (‰) of Fine particle organic matter mass; C. Δδ 15N (‰) of filter feeder
(Culex sp.); D. Δδ 15N (‰) of detritivores (Scirtes sp.); E. Δδ15N (‰) of thepredator
(O. oreas). Precipitation treatments correspond to 0.1X, 1X and 3x of the rainfall mean.
Predator treatment correspond presence or absence of predator (O.
12 ACKNOWLEDGMENTS
First, I wish to express my sincere thanks to my advisor, Emilio Realpe, for giving me
the opportunity to do my PhD within the LAZOEA (Laboratorio de Zoología y Ecología
Acuática). He has given so much of himself to help me succeed. My sincere thanks to
my external advisor Diane Srivastava, professor of Department of Zoology, University
of British Columbia, for many fruitful discussions and ideas for my research; I am
extremely thankful and indebted to her for sharing her ability, and for the sincere and
valuable guidance and encouragement extended to me.
I am grateful to the Department of Biological Sciences of the Universidad de Los Andes
and the Proyecto Semilla Facultad de Ciencias at the Universidad de Los Andes for
providing me with all the necessary facilities for the research. This doctorat would not
have been possible without the economic support of COLCIENCIAS (Doctorado
Nacional 567).
I would also like to express my thanks to Aguas de Manizales for the opportunity to
develop the thesis at the Reserva Forestal Protectora Rio Blanco y Quebrada Olivares.
I am also grateful to University of Utah for giving me the opportunity to take part in
ISOCAMP 2012, and to the ITEC (Inter-university Training for Continental- Scale Ecology) for the fellowship of the project “Effects of drought over nitrogen and energy
flux in a food web”. I would also like to express my sense of gratitude to Jed P. Sparks, Director of the Cornell Isotope Laboratory (COIL) and professor of Ecology or
Evolutionary Biology at the University of Cornell, and to Kimberlee Sparks, Cornell
13 analysis of stable isotope and discussion about stable isotope.
I also thank Kurtis Trzcinski, postdoc student at the University British Columbia, who
helped in the field and for his suggestion in the precipitation regime research. I take this
opportunity to express my gratitude to all field assistants for their help and support in
the field station.
14 OBJETIVES
GENERAL OBJETIVES
Assess the effects of the hydrological regimen and spatial scale on invertebrate
communities and ecosystem processes of phytotelmata.
SPECIFIC OBJETIVES
Characterize the invertebrate community associated to Guzmania
multiflora (Bromeliaceae) in Cloud Mountain.
Assess the scale dependence of habitat and litter type effects on tree
holes communities.
Assess the scale dependence of habitat and litter type effects on
decomposition processes.
Determine the changes in community and ecosystem processes produced
by a change in the frequency and magnitude of rainfall.
Assess the effects of rainfall magnitude and trophic structure on energy
15 CHAPTER 1. INTRODUCTION
Phytotelmata are small aquatic habitats formed by different plant structures such as leaf
axils, fruits, flower parts, or tree trunks and branches (Fish, 1983; Kitching, 2000).
Examples of phytotelmata include pitcher plants, bamboo internodes, tree holes, and
tank bromeliads (Kitching, 2001). Bromeliads and tree holes are the most abundant
phytotelmata in the Neotropics; the rosette disposition of bromeliad leaves creates a
tank that allows accumulation of rainwater and detritus from the canopy. The rainwater
reserve, however, is not constant throughout the bromeliad, thus, the bromeliad provides
two habitats for fauna: the young leaf axils maintain water in their interior forming an
aquatic habitat, whereas water is lost by older or mature leaves in the outer part of
bromeliad provides a terrestrial habitat (Araujo et al., 2007; Montes de Oca et al., 2007;
Frank, 1983). Tree holes are formed by the rainwater catchment of decomposing
cavities or depressions in the woody portions of trees (Kitching, 1971). Tree holes
receive organic material from trapped dead leaves and inorganic ions from stem flow
(Eaton et al., 1973).
Overall, phytotelmata contain small volumes of water and detritus that allow the
maintenance of associated communities (Fish, 1983; Maguire, 1970; Srivastava et al.,
2004). The chemical features of water are influenced by decomposing plant material
and the metabolic activity of organisms (Ngai and Srivastava, 2006); therefore, water in
phytotelmata has low oxygen concentration and an acidic pH (Laessle, 1961).
Phytotelmata are characterized by a defined area as a discrete and replicable unit
16 community on a temporal and spatial scale (Kitching, 1971). They contain fauna with
short life cycles (Srivastava et al., 2004) and, in some cases, only a part of the life cycle
is developed in the phytotelmata, allowing species dispersion and energy flux between
phytotelmata and terrestrial ecosystems (Giller et al., 2004). Phytotelmata have lower
species richness than macroecosystems, allowing a clearly defined food web. These
characteristics have led to an increase in phytotelmata studies focused on ecosystem,
community, and population ecology, showing the relevance of these microecosystems
in ecology.
The first studies on bromeliads and tree holes focused on species reports, especially of
taxonomic groups such as damselflies and mosquitoes (Frank, 1983; Galindo et al.,
1950, 1951, 1955; Kitching, 1971;Laessle, 1961; Lounibos et al., 1987; Picado, 1913;
Pittendrigh, 1948 ). These studies and others have reported that communities in
bromeliads and tree holes are characterized by bacteria (Brighigna et al., 1992 ;Goffredi
et al., 2011a,b; Vega-Sepulveda, 2009), algae, flagellates, ciliates (Carrias, 2001;
Durán-Ramírez et al., 2015), arthropods, and vertebrates (Neill, 1951). Arthropods
show high diversity and abundance in bromeliads and tree holes (Kitching, 2000; Liria,
2007; Ospina-Bautista et al., 2004; Ospina-Bautista et al., 2008; Richardson et al.,
2000; Williams, 2006; Yanoviak et al., 2006a), with the orders Diptera (Cranstron,
2007; Derraik, 2005; Epler and Janetzky, 1998; Frank and Lounibos, 2009; Wagner et
al., 2008), Odonata (Corbet, 1983; De Marmels and Garrison, 2005; Melnychuk and
Srivastava, 2002), Hemiptea (Polhemus and Polhemus, 1991), Coleoptera (Blake et al.,
2008; Ospina–Bautista et al., 2004), Collembola, Orthoptera (Frank et al., 2004),
Blattodea, and Dermaptera (Frank and Lounibos, 2009). Moreover, diplopods,
17 2005), mites (Frank et al., 2004), scorpions, and pseudo scorpions (Frank et al., 2004;
Richardson, 1999) have been reported.
These organisms are important for nutrient cycling and ecosystem processes. Terrestrial
fauna that visit the bromeliad, such as ants, spiders, and frogs, may contribute to
nitrogen cycling by depositing nitrogen to the bromeliad through their feces (Leroy et
al., 2009; Romero et al., 2010; Romero and Srivastava, 2010). Moreover, predation
activity of damselflies (Mecistogaster modesta) retains the nitrogen that can be lost
through detritivorous emergence on bromeliads; therefore, damselflies are an important
element of the nitrogen flux from leaf litter to the bromeliad (Ngai and Srivastava,
2006). Predators in bromeliads and their interactions may affect the carbon cycle
through their influence on carbon dioxide concentrations in bromeliads; for example,
damselflies reduce carbon dioxide concentration, but their interaction with another
predator (Copelatus sp.) eliminates top-down influences on the carbon cycle (Atwood et
al., 2014). In addition, bacteria such as Methanomicrobiales, Methanocelales, and
Metanosarcinales release methane as a result of decomposition processes, turning the
bromeliad into a methane source (Goffredi et al., 2011b).
Bromeliad and tree holes communities have been used to assess the abiotic and biotic
factors that determine communities and populations. Overall, researchers have found
that habitat characteristics are the most relevant factors determining populations and
community structure. For instance, habitat size determines spider assemblages,
protozoa, algal, and invertebrate communities (Goncalves-Souza et al., 2011; Carrias et
al., 2001; Carrias et al., 2014; Frank, 2004;), as well as the population density of
18 holes (Yanoviak, 1999), and Culex biscaynensis in exotic bromeliads (O’Meara et al.,
2003). Tree hole depth and height determine mosquito distribution (Copeland and
Craig, 1990) and relevant characteristics of oviposition selection (Sinsko and
Grimstand, 1977). In addition, habitat complexity, measured through leaf number,
determines algal, protozoa, and invertebrate communities, showing a positive relation
with protozoa richness and invertebrate communities, and a negative relation with algal
communities (Armbruster et al., 2002; Carrias, 2001; Carrias et al, 2012; Jabiol et al.,
2009). Moreover, bromeliad leaf architectures affect the presence of Psecas chapoda
(Salticidae) (O’mena and Romero, 2008). Finally, habitat location influences the
abundance and richness of invertebrates associated with tree holes and is related to
habitat selection by adults (Fincke and Yanoviak, 1997).
Likewise, water volume and its physicochemical features can affect populations or
communities. Water volume in phytotelma has a positive relation with invertebrate and
algal richness and abundance (Araujo, 2007; Carrias et al., 2014; Dézerald et al., 2014;
Jabiol et al., 2009; Kitching, 2001;Yanoviak et al., 2006a), as well as Chironomidae
abundance (Sodré et al., 2010) and Culicidae assemblages (Marques et al., 2012).
Variation in pH appears to be a relevant condition for bacteria and insects; in this
regard, Alphaproteobacteria, Acidobacteria, Planctomycetes, Bacteroidetes,
Betaproteobacteria, Firmicutes, and Bacteroidetes of bromeliads in Costa Rica show a
positive or negative relation to water pH according to the bacterial species (Goffredi et
al., 2011a); for example, a low pH leads to slow growth of Helodes pulchella (Paradise,
19 Detritus is the main base resource in tree holes and bromeliads, and strongly influences
freshwater faunal communities (Dézerald et al., 2014). Studies have found that low
quality and quantity of this resource leads to lower invertebrate richness and abundance
(Fish and Carpenter, 1982; Richardson, 1999). However, Srivastava and Lawton (1998)
found that an increase in detritus leads to more species, but not greater abundance in
tree holes. Detrital variations shift oviposition of mosquitoes such as Aedes albopictus
and Aedes aegypti (Fader and Juliano, 2014). Detrital quantity alters the growth and
survival of Helodes pulchella, which shows slower growth when fed less detritus, but
reduced survival under high detrital amounts in tree holes (Paradise, 1999).
Chironomidae and Tricoptera growth in bromeliads is limited by the nutrients in leaf
litter (Gonzalez et al., 2014). Moreover, high values of fine particule organic matter
(FPOM) lead to an increase protozoan richness (Carrias et al., 2012).
Bromeliads and tree holes communities have been used to assess the effects of
predation, herbivory and facilitation on species and communities. Aquatic predators
reduce the abundance and richness of invertebrates (Yanoviak, 2001a), rotifers, and
protozoa (Kneitel and Chase, 2011) in tree holes, whereas spiders regulate abundance
and diversity of invertebrates that carry out their entire life cycle in bromeliad water
(Romero and Srivastava, 2010). Predation also affects population dynamics; for
instance, a top predator (Toxorhynchites rutilus) reduces survivorship of prey species
and intermediate predators (Corethrella appendiculata), changing prey composition in
tree holes (Griswold and Lounibos, 2006). Mecistogaster modesta (top predator) shows
a similar effect on Chironomidae emergence (collector-gatherer) (Starzomski et al.,
2010) and mosquitos in bromeliads (Hammill et al., 2015), while the feeding activity of
20 by the bromeliad-eating weevil (Metamasius callizona) decreases the abundance of
Tillandsia utriculata in the canopy, reducing available aquatic habitats for communities
(Cooper et al., 2014).
Facilitation processes have been reported for bromeliads and tree holes. In bromeliads,
detritivory facilitates the emergence of Chironomidae (Starzomski et al., 2010);
furthermore, ciliate communities change with the loss of detritivore diversity when the
top predator is extinct (Srivastava and Bell, 2009). The presence of ants (Camponotus
femoratus) produces greater richness and abundance of protists (Carrias et al., 2012),
and frogs and snakes help to disperse ostracods (Serramo et al., 1999). In tree holes,
feeding by Scirtidae beetles indirectly facilitates mosquito production through the
microbial community (Daugherty and Juliano, 2003; Pelz-Stelinski et al., 2011).
Climatic conditions and anthropogenic effects lead to habitat loss and altered water and
nutrient cycles and availability of bromeliads and tree holes. Climatic conditions such as
hurricanes decrease the alpha and beta diversity of associated invertebrates, since
hurricanes reduce bromeliad density and rare species (Richardson et al., 2015). Drought
has the greatest effects on diversity and abundance of tree holes insects within forest
patches and bromeliads (Amundrud and Srivastava, 2015; Srivastava, 2005), while
anthropogenic effects such as deforestation, land use, and pollution produce shifts in
communities. For instance, deforestation increases the abundance of mosquitoes in tree
holes (Yanoviak et al., 2006b), land use leads to different community composition
(Yanoviak et al., 2006b); and pollutant as pentachlorophenol alters the bacterial
21 In summary, phytotelmata are micro-aquatic ecosystems in terrestrial ecosystems with
special features that allow them to harbour an important diversity of bacteria, protists,
invertebrates, and vertebrates that support ecosystem processes; therefore, phytotelmata
could be used as an ecological model (Srivastava et al., 2004). As phytotelmata,
bromeliads and tree holes could be relevant to assess the effect of the hydrological
regimen and spatial scale on phytotelmata communities.
1.1. REFERENCES
Ager, D., Evans, S., Li, H., Lilley, A.K. and Van der Gast, C.J. 2010. Anthropogenic
disturbance affects the structure of bacterial communities. Environmental Microbiology
12:670-678.
Araujo, V., Melo, S., Araujo, A., Gomes, M. and Carneiro, M. 2007. Relationship
between invertebrate fauna and bromeliad size. Brazilian Journal of Biology 67:611–
617.
Amundrud, S.L., Srivastava, D.S., and O'Connor, M.I. 2015. Indirect effects of
predators control herbivore richness and abundance in a benthic eelgrass (Zostera
marina) mesograzer community. Journal of Animal Ecology 84(4): 1092-1102.
Armbruster, P., Hutchinson R.A. and Cotgreave, P. 2002. Factors influencing
22 Atwood, T.B., Hammill, E., Srivastava, D.S. and Richardson, J.S. 2014.Competitive
displacement alters top-down effects on carbon dioxide concentrations in a freshwater
ecosystem. Acta Oecologia 175:353–361.
Blake, M., Gómez-Zurita, J., Ribera, I., Vitoria, A., Zillikens, A., Steiner, J., García, M.,
Hendrich, L. and Vogler, A.P. 2008. Ancient associations of aquatic beetles and tank
bromeliads in the Neotropical forest canopy. Proceedings of the National Academy of
Sciences 105:6356–6381.
Brighigna, L., Montaini, P., Favilli, F. and Trejo, A.C. 1992. Role of the
nitrogen-fhxing bacterial microflora in the epiphytism of Tillandsia (Bromeliaceae). Journal of
Botany 79:723–727.
Carrias, J.F., Cereghino, R., Brouard, O., Pelozuelo, L., Dejean, A., Coute, A., Corbara,
B. and Leroy, C. 2014. Two coexisting tank bromeliads host distinct algal communities
on a tropical inselberg. Plant Biology 16:997–1004.
Carrias, J.F., Brouarda, O., Leroy, C., Céréghino, R., Pélozuelod, L., Dejean, A.,
Corbara, B. 2012. An ant–plant mutualism induces shifts in the protist community
structure of a tank-bromeliad. Basic and Applied Ecology 13:698–705.
Carrias, J., Cussac, M.E. and Corbara, B. 2001. A preliminary study of freshwater
23 Cooper, T.M., Frank, J.H. and Cave, R.D. 2014. Loss of phytotelmata due to an
invasive bromeliad-eating weevil and its potential effects on faunal diversity and
biogeochemical cycles. Acta Oecologica 54:51–56.
Copeland, R.S. and Craig, G.B. Jr. 1990. Habitat segregation among treehole
mosquitoes (Diptera: Culicidae) in the Great Lakes region of the United States. Annals
of the Entomological Society of America 83:1O63-1O73.
Corbet, P.S. 1983. Odonata in phytotelmata. En: Frank, J.H. and Lounibos, L.P., (eds.)
Phytotelmata: terrestrial plants as hosts for aquatic insect communities. Plexus
publishing, New Jersey. 29-54p.
Cranston, P.S. 2007. New Species for a Bromeliad Phytotelm-Dwelling Tanytarsus (Diptera : Chironomidae). Annals of the Entomological Society of America 100:617–
622.
Daugherty, M.P. and Juliano, S.A. 2003. Leaf-scraping beetle feces are a food resource
for treehole mosquito larvae. American Midland Naturalist 150:181–184.
De Marmels, J. and Garrison, R.W. 2005. Review of the genus Leptagrion in Venezuela
with new synonymies and descriptions of a new genus, Bromeliagrion, and a new
species B. rehni (Zygoptera: Coenagrionidae). The Canadian Entomologist 137:257–
24 Derraik, J.G.B. 2005. Mosquitoes breeding in phytotelmata in native forests in the
Wellington region, New Zealand. New Zealand Journal Ecology 29:185–191.
Dézerald, O., Talaga, S., Leroy, C., Carrias, J.F., Corbara, B., Dejean, A., Cereghino, R.
2014. Environmental determinants of macroinvertebrate diversity in small water bodies:
Insights from tank-bromeliads. Hidrobiologica 723:77–86.
Durán-Ramírez, C.A., García-Franco, J.G., Foissner, W. and Mayén-Estrada, R. 2015.
Free-living ciliates from epiphytic tank bromeliads in Mexico. European Journal of
Protistology 51:15–33.
Eaton, J.S., Likens, G.E. and Bormann, F.H. 1973. Throughfall and stem-flow
chemistry in a northern hard- wood forest. Journal of Ecology61:495-508.
Epler, J.H. and Janetzky, W.J. 1998. A new species of Monopelopia (Diptera:
Chironomidae) from phytotelmata in Jamaica, with preliminary ecological notes.
Journal of the Kansas Entomological Society 71:216–225.
Fader, J.E. and Juliano, S.A. 2014. Oviposition habitat selection by container-dwelling
mosquitoes: Responses to cues of larval and detritus abundances in the field. Ecological
Entomology 39:245–252.
Fincke, O., Yanoviak, S.P. 1997. Predation by odonates depresses mosquito abundance
25 Fish, D. 1983. Phytotelmata: Flora and Fauna. En: Frank, J.H. and Lounibos, L.P.,
(eds.) Phytotelmata: terrestrial plants as hosts for aquatic insect communities. Plexus
publishing, New Jersey. 1-25p.
Fish, D. and Carpenter, S.R. 1982. Leaf litter and larval mosquito dynamics in tree-Hole
ecosystems. Ecology 63:283–288.
Frank, J.H. and Lounibos, L.P. 2009. Insects and allies associated with bromeliads: a
review. Terrestrial Arthropod Reviews 1: 125–153.
Frank, J.H., Reenivasan, S.S., Benshoff, P.J., Deyrup, M.A., Edwards, G.B., Halbert,
S.E., Hamon, A.B., Lowman, M.D., Mockford, E.L., Scheffrahn, R.H., Steck, G.J.,
Thomas, M.C., Walker, T.J. and Welbourn, W.C. 2004. Invertebrate animals extracted from native tillandsia (Bromeliales : Bromeliaceae) in Sarasota County, Florida. Florida
Entomological 87:176–185.
Frank, J.H. 1983. Bromeliad phytotelmata and their biota, especially mosquitos,
pp.101-128. En: Frank, J.H., Lounibos, L.P. (eds) Phytotelmata: terrestrial plants as hosts of
aquatic insects communities. Plexus publishing, New Jersey. 293p.
Galindo P., Carpenter, S.J. and Trapido, H. 1955. A contribution to the ecology and
biology of tree hole breeding mosquitoes of Panama. Annals of the Entomological
26 Galindo, P., Carpenter, S.J. and Trapido, H. 1951. Ecological observations on forest
mosquitoes of an endemic yellow fever area in Panama. The American Journal of
Tropical Medicine and Hygiene 31:98-137.
Galindo, P., Carpenter, S.J. and Trapido, H. 1950. Observations on diurnal forest
mosquitoes in relation to sylvan yellow fever in Panama. The American Journal of
Tropical Medicine and Hygiene 30:533-574.
Giller, P.S., Hillebrand, H., Berninger, U.G., Gessner, M.O., Hawkins, S., Inchausti, P.,
Inglis, C., Leslie, H., Malmqvist, B., Monaghan, M.T., Morin, P.J. y O’Mullan, G.
2004. Biodiversity effects on ecosystem functioning: emerging issues and their
experimental test in aquatic environments. Oikos 104:423-436.
Goffredi, S.K., Kantor, A.H., and Woodside, W.T. 2011a. Aquatic microbial habitats
within a neotropical rainforest: bromeliads and pH-associated trends in bacterial
diversity and composition. Microbial Ecology 61:529-542.
Goffredi, S.K., Jang, G.E., Woodside, W.T. and Ussler, W. 2011b. Bromeliad
catchments as habitats for methanogenesis in tropical rainforest canopies. Frontiers in
Microbiology 2:256.
Goncalves-Souza, T., Almeida-Neto, M. and Romero, G.Q. 2011. Bromeliad
architectural complexity and vertical distribution predict spider abundance and richness.
27 Gonzalez, A.L., Romero, G. and Sirivastava, D.S. 2014. Detrital nutrient content
determines growth rate and elemental composition of bromeliad-dwelling insects.
Freshwater Biology 59:737–747.
Griswold, M.W. and Lounibos, L.P. 2006. Predator identity and additive effects in a
treehole community. Ecology 87:987–995.
Hammill, E.D.D., Atwood, T.B., Corvalan, P. and Srivastava, D.S. 2015. Behavioural
responses to predation may explain shifts in community structure. Freshwater Biology
60:125–135.
Jabiol, J., Corbara, B., Dejean, A. and Céréghino, R. 2009. Structure of aquatic insect
communities in tank-bromeliads in a East-Amazonian rainforest in French Guiana.
Forest Ecology and Management 257:351–360.
Kitching, R.L. 2001. Food webs in phytotelmata: “Bottom-Up” and “Top-Down”
explanations for community structure. Annual Review of Entomology 46:729-760.
Kitching, R.L., 2000. Food webs and container habitats: the natural history and ecology
of Phytotelmata. Cambridge University Press, Cambridge. 431p.
Kitching, R.L. 1971. An ecological study of water-filled tree-holes and their position in
28 Kneitel, J.M. and Chase, J.M. 2011. Disturbance, predator, and resource interactions
alter container community composition. Ecology 85:2088–2093.
Laessle, A.M. 1961. A Micro-Limnological Study of Jamaican Bromeliads. Ecology
42:499–517.
Leroy, C., Corbara, B., Dejean, A. and Cereghino, R. 2009. Ants mediate foliar
structure and nitrogen acquisition in a tank- bromeliad. New Phytologist 183:1124–
1133.
Liria, J. 2007. Fauna fitotelmata en las bromelias Aechmea fendleri André y
Hohenbergia stellata Schult del Parque Nacional San Esteban, Venezuela. Revista
Peruana de Biología 14:33–38.
Lounibos, L.P., Frank, J.H., Machado–Allison, C.E., Navarro, J.C. and Ocanto, P. 1987.
Seasonality, abundance and invertebrate associates of Leptagrion siqueirai Santos
in Aechmea bromeliads in Venezuelan rain forest (Zygoptera:
Coenagrionidae). Odonatologica 16:193–199.
Maguire, B. 1970. Aquatic communities in bromeliad leaf axils and the influence of
radiation. Pp. E.95–E101. En: Odum, H.T. and Pigeon, R.F. (eds). A tropical rain forest.
A study of irradiation and ecology at El Verde, Puerto Rico. Division of Technical
29 Marques, T.C., Bourke, B.P., Laporta, G.Z. and Sallum, M.A.M. 2012. Mosquito
(Diptera: Culicidae) assemblages associated with Nidularium and Vriesea bromeliads in
Serra do Mar, Atlantic Forest, Brazil. Parasites and Vectors 5:41.
Melnychuk, M.C and Srivastava, D.S. 2002. Abundance and vertical distribution of a
bromeliad-dwelling zygopteran larva, Mecistogaster modesta, in a Costa Rican
rainforest (Odonata: Pseudostigmatidae). International Journal of Odonatology 5:81–97.
Montes de Oca, E., Ball, G.E. and Spence, J.R. 2007. Diversity of Carabidae (Insecta,
Coleoptera) in epiphytic Bromeliaceae in Central Veracruz, Mexico. Environmental
Entomology 36:560–568.
Neill, W.T. 1951. A Bromeliad herpetofauna in Florida. Ecological Society of America
32:140–143.
Ngai, J.T. and Srivastava, D.S. 2006. Predators accelerate nutrient cycling in a
Bromeliad Ecosystem. Science 314:963.
O’Meara, G.F.O., Cutwa, M.M. and Evans, L.F. 2003. Bromeliad-inhabiting
mosquitoes in south Florida: native and exotic plants differ in species composition.
Journal of Vector Ecology 28:37–46.
O’mena, P.M. and Romero G.Q. 2008. Fine-scale microhabitat selection in a
bromeliad-dwelling jumping spider (Salticidae). Biological Journal of the Linnean Society 94:653–
30 Ospina-Bautista, M.F., Estevez-Varón, J.V., Betancur, J. and Realpe, E. 2004.
Macroinvertebrados acuáticos asociados a la bromelia Tillandsia turneri en un bosque
altoandino. Revista Acta Zoológica Mexicana 20(1):153-166.
Ospina-Bautista, M.F., Estevez-Varon, J.V., Realpe, E. and Gast, F. 2008. Diversidad
de invertebrados acuáticos asociados a Bromeliaceae en un bosque de montaña. Revista
Colombiana de Entomología 34(2):224-229.
Paradise, C.J. 2000. Effects of pH and resources on a processing chain in simulated
interaction treeholes. British Ecological Society 69:651–658.
Paradise, C.J. and Kuhn, K.L. 1999. Interactive effects of pH and leaf litter on a
shredder, the scirtid beetle, Helodes pulchella, inhabiting tree-holes. Freshwater
Biology 41:43–49.
Pelz-Stelinski, K.S., Kaufman, M.G. and Walker, E.D. 2011. Beetle (Coleoptera: Scirtidae) facilitation of larval mosquito growth in tree hole habitats is linked to
multitrophic microbial interactions. Microbial Ecology 62:690-703.
Picado, C. 1913. Les broméliacées épiphytes considerées comme milieu biologique.
Bulletin des Sciences de la France et de la Belgique 47:215–360.
Pittendrigh, C.S. 1948. The bromeliad-Anopheles-malaria complex in Trinidad; The
31 Polhemus, J.T. and Polhemus, D.A. 1991. A review of the veliid fauna of bromeliads
with a key and description of a new species (Heteroptera Veliidae). Journal of the New
York Entomological Society 99:204–216.
Richardson, M.J., Richardson, B.A. and Srivastava, D.S. 2015. The Stability of
invertebrate communities in bromeliad phytotelmata in a rain forest subject to
hurricanes. Biotropica 47:201–207.
Richardson, B.A., Rogers, C. and Richardson, M.J. 2000. Nutrients, diversity, and
community structure of two phytotelm systems in a lower montane forest, Puerto Rico.
Ecological Entomology 25:348–356.
Richardson, B.A. 1999. The Bromeliad microcosm and the assessment of faunal
diversity in a neotropical forest.Biotropica 31(2): 321-336.
Romero, G.Q. and Srivastava, D.S. 2010. Food-web composition affects
cross-ecosystem interactions and subsidies. Journal of Animal Ecology 79:1122–1131.
Romero, G.Q., Nomura, F., Gonçalves, A.Z., Dias, N., Mercier, H., Conforto, E. de C.,
Rossa-Feres, D. de C. 2010. Nitrogen fluxes from treefrogs to tank epiphytic
bromeliads: An isotopic and physiological approach. Acta Oecologia 162:941–949.
Romero, G.Q. and Vasconcellos-Neto, J. 2005. Spatial distribution and microhabitat
32 Arachnology 33:124–134.
Serramo-Lopez, L.C., Pena-Rodrigues, P.J.F. and Iglesias-Rios, R. 1999. Frogs and
snakes as phoretic dispersal agents of bromeliad ostracods (Limnocytheridae: Elpjdium)
and annelids (Naididae: Dero). Biotropica 31:705–708.
Sinsko, M.J. and Grimstad, P.R. 1977. Habitat separation by differential vertical
oviposition of two treehole Aedes in Indiana. Environmental Entomology 6:485-487.
Sodré, V.M., Rocha, O. and Messias, M.C. 2010. Chironomid larvae inhabiting
bromeliad phytotelmata in a fragment of the Atlantic Rainforest in Rio de Janeiro State.
Brazilian Journal of Biology 70(3):587-92.
Srivastava, D.S. and Bell, T. 2009. Reducing horizontal and vertical diversity in a food
web triggers extinctions and impacts functions. Ecology Letters 12:1016–1028.
Srivastava, D.S. 2005. Do local processes scale to global patterns? The role of drought
and the species pool in determining treehole insect diversity. Acta Oecologia 145:205–
215.
Srivastava D.S, Kolasa, J., Bengtsson, J., Gonzalez, A., Lawler, S.P., Miller, T.E.,
Munguia, P., Romanuk, T., Schneider, D.C. and Trzcinski, M.K. 2004. Are natural
microcosms useful model systems for ecology?.Trends in Ecology and Evolution 19(7):
33 Srivastava, D.S. and Lawton, J.H. 1998. Why more productive sites have more Species :
An experimental test of theory using tree-hole communities. The American Naturalist
152:510–529.
Starzomski, B.M., Suen, D. and Srivastava, D.S. 2010. Predation and facilitation
determine chironomid emergence in a bromeliad-insect food web. Ecological
Entomology 35:53–60.
Vega-Sepulveda, J.A. 2009. Bacterias fototróficas anoxigénicas púrpuras no-sulfurosas
en la fitotelmata de bromelias en diversos bosques de Puerto Rico. Tesis Maestría,
Universidad de Puerto Rico, Recinto Universitario de Mayagüez. Puerto Rico. 104 pp.
Wagner, R., Richardson, B.A. and Richardson, M.J. 2008. A new psychodid species
from Puerto Rican tank bromeliads. Studies on Neotropical Fauna and Environment
43:209–216.
Walker, E.D., Lawson, D.L., Merritt, R.W., Morgan, W.T. and Klug, M.J.
1991. Nutrient dynamics, bacterial-populations, and mosquito productivity in tree hole
ecosystems and microcosms. Ecology 72:1529–1546.
Williams, D. 2006. The Biology of Temporary Waters. University of Toronto at
34 Yanoviak, S.P., Lounibos, L.P. and Weaver, S.C. 2006a. Land use affects
macroinvertebrate community composition in phytotelmata in the peruvian amazon.
Annals of the Entomological Society of America 99(6):1172–1181.
Yanoviak, S.P., Ramírez-Paredes, J.E., Lounibos, L.P. and Weaver, S.C. 2006b.
Deforestation alters phytotelm habitat availability and mosquito production in the
peruvian amazon. Ecogical Applications 16:1854–1864.
Yanoviak, S.P. 2001.. Predation, resource availability, and community structure in
Neotropical water-filled tree holes. Acta Oecologia 126:125–133.
Yanoviak, S.P. 1999. Distribution and abundance of Microvelia cavicola Polhemus
(Heteroptera: Veliidae) on Barro Colorado Island, Panama. Journal of the New York
35 CHAPTER 2. INVERTEBRATE COMMUNITY ASSOCIATED TO GUZMANIA
MULTIFLORA (BROMELIACEA) IN CLOUD MOUNTAIN: HABITAT
COMPLEXITY AND AVAILABLE ENERGY AFFECTS BIOLOGICAL TRAITS.
2.1. ABSTRACT
Habitat complexity and available energy are among the most important factors
structuring communities. Moreover, these factors could determine the biological traits
of organisms in a community, thus, altering ecosystem processes. We studied the
relation between habitat complexity and resource availability and the biological traits of
the invertebrate community in Guzmania multiflora (André) André ex Mez.
(Bromeliaceae), using leaf number and the amount of litter contained as measures of
habitat complexity and available energy, respectively. We collected the inhabiting
invertebrates and determined their biological traits (habitat, stage, functional group, and
dispersal type). We found that habitat complexity not only alters the taxonomical
diversity of invertebrates in bromeliads, but also their functional diversity through
changes in the abundance and richness of biological traits. In conclusion, biological
traits provide an approach to ecosystem processes and invertebrate adaptations to
environmental conditions; therefore, the study of changes in the abundance and richness
of biological traits could contribute key tools to study the effects of climate change and
anthropogenic disturbances on ecosystems.
2.2. INTRODUCTION
Habitat complexity and available energy are among the most important factors
structuring communities (Hurlbert, 2004). Habitat complexity alters the richness and
36 more complex habitats (Kovalenko et al., 2012). This tendency has been explained
through the niche space hypothesis, which states that complex habitats give more niche
space to species (Willis et al., 2005), and through the resilience hypothesis where
habitat complexity could lead to an increased efficiency in utilizing resources and
providing greater resilience to communities from disturbances (Kovalenko et al., 2012).
On the other hand, energy availability could determine the number of species in
communities (Species-energy theory, Wright, 1983; Tittensor et al., 2011) by increasing
the number of individuals in the community, reducing the stochastic risk of species
extinction, and supporting more species (Srivastava and Lawton, 1998; Hurlbert, 2006),
or by a high resource abundance that can promote the occurrence of specialist species
increasing richness and reducing competition (Evans et al., 2005).
Moreover, habitat complexity and resource availability can alter ecosystem processes.
The effect of habitat complexity on ecosystem processes is poorly known (Tokeshi and
Arakaki, 2012) in spite of the potential of habitat complexity to alter food webs, energy
flux, and resilience and resistance of ecosystems to perturbations (Kovalenko et al.,
2012; Floater, 2001). On the contrary, the effects of resource availability on ecosystem
processes is well known, such as on decomposition, food webs, and primary
productivity (Davis et al., 2000; Moore et al., 2004; Fretwell, 1987).
Habitat complexity and resource availability could determine the biological traits of
organisms in a community; therefore, altering ecosystem processes. Biological traits are
organism characteristics at a morphological, physiological, biochemical, phenological,
37 (Violle et al., 2007) and include body size, locomotion, reproduction, dispersion, and
trophic group (Heino, 2005). Organisms and biological communities influence
ecosystem processes though functional traits (Bello et al., 2010). For example, leaf
traits such as specific leaf area, tensile strength, leaf chemistry, and macroinvertebrate
traits such as body size of detritivores are related with decomposition process (Birouste,
et al., 2012; Gurvich et al., 2003); aerial respiration of invertebrates is related with
oxygen depletion (Dolédec et al., 2006); body size, dispersal ability, and mobility of
invertebrates are related with pest regulation; body size of soil invertebrates is related
with soil stability and fertility (Bello et al., 2010); and, finally, body size is related with
structure and dynamics of food webs (Woodward et al., 2005).
Bromeliad and their fauna can be relevant to assess the effects of habitat complexity and
energy availability on communities and their biological traits, since bromeliads show
variation in both complexity and energy inputs. In terms of complexity, bromeliads
have interlocking leaves where litter and rainfall are accumulated. Moreover, algae,
bacteria, protists, and arthropods live in bromeliad tanks (Benzing, 1990; Brouard et al.,
2012), creating a food web based on detritus and algae (Brouard et al., 2011). Habitat
complexity in bromeliads is measured through leaf number that is related with the
available tank or well number and size of the bromeliad; leaf number joint two aspect of
the habitat complexity the quantitative and qualitative (Stoners and Lewis, 1985). The
amount of litter of allochthonous origin is the principal detrital energy input in
38 In this paper, we explored the relation between habitat complexity and resource
availability and the biological traits of the invertebrate community in bromeliads. We
tested the hypothesis that habitat complexity and resource availability not only affect
diversity, but also the functional traits of invertebrates such as stage, functional groups,
and dispersal ability. A complex habitat and high resource availability is predicted to
support more species and affect the diversity of biological traits. Moreover, we
predicted differences in abundance and richness between categories of biological traits,
due to adaptations of invertebrates related to colonizing this microecosystem.
2.3. METHODS
2.3.1. Study Area
The study was conducted at the Reserva Forestal Protectora of the Rio Blanco and
Quebrada Olivares Hydrographical Basins. The 4932-ha reserve is located on the western slope of the Central Mountain Range in Colombia (05°3’ 96.7’’ N;
75°26’’88.4’’ W), with a secondary forest and an Alder plantation between 2150 and
3700 m.a.s.l. The maximum annual average temperature is 19°C and the minimum is
6.9°C and the annual mean precipitation is 2500 mm.The most abundant plant families
are Araceae, Actinidaceae, Boraginaceae, and Cyatheaceae.
2.3.2. Methods
We collected individuals of Guzmania multiflora (André) André ex Mez between one
and four meters aboveground. We measured leaf number and the amount of litter
39 Bromeliad leaves were removed and the water was filtered to collect the inhabiting
invertebrates. The invertebrates were preserved in 70% alcohol and taxonomically
identified to the highest taxonomic level possible using general references: Merrit and
Cummins, 2008; Dominguez and Fernandez, 2009; Stehr, 2005. The biological traits
assessed for the invertebrates were determined by direct observation and the literature.
The biological traits and categories used were: habitat (aquatic, terrestrial), stage (adult,
larvae), functional group (predators, shredders, filter feeders, scrapers, and piercers),
and dispersal type (aerial active, terrestrial active, and aerial passive). Trait abundance
was calculated as the number of individuals per category in each trait, while richness
was calculated as the number of species that had in a given category of a biological trait.
The data was transformed as log (x + 1) for richness and abundance and as log (x) for
leaf number and litter mass.
2.3.3. Statistical analysis
Multiple linear regressions (LM) were used to assess the relation between resource
availability and habitat complexity on taxonomical and biological traits diversity. The
models predicted either richness or abundance of invertebrates associated to bromeliads
or a category of functional trait. We performed a linear regression with all of the
possible combinations of the leaf number and litter amount variables; subsequently, we
selected the best model by the AIC criterion. To compare abundance and richness of the
categories for each biological trait, we conducted a student t-test or ANOVA, if the
traits had more than two categories, by previously verifying assumptions. The
statistical analyses were conducted with the R statistical program.
40 2.4. RESULTS
We found 4375 macroinvertebrate individuals distributed in 62 morphospecies, of
which 41.93% were aquatic and 61.53% consisted of immature stages. The order
Diptera dominated the community associated to Guzmania multiflora, with the families
Culicidae, Chironomidae, and Syrphidae; however, the most abundant morphospecies
was Scirtes sp. (Coleoptera) with 2439 individuals. Formicidae, Aranea, and Ligidae
were the most frequent terrestrial fauna in Guzmania multiflora (Table 2.1, Figure 2.1).
Abundance and richness differed in relation to habitat complexity; bromeliads with
greater leaf number harbored a higher macroinvertebrate abundance (LM: F2,28= 5.222,
p= 0.011, r2=0.219; log (leaf number) t= 2.344, p= 0.026; log (litter mass) t= 0.762, p=
0.452 and richness (LM: F 2,28= 6.601, p= 0.004, r2=0.271; log (leaf number) t= 3.485,
p= 0.001; log(litter mass) t= -0.843, p= 0.406) (Figure 2.2 A,B).
The categories of biological traits differed in their abundance and/or richness. We
found more abundance of aquatic (t-student; t= -7.084, p= 1.42e-9, df= 63) and
immature invertebrates (t–student; t= -7.094, p= 1.36e-9, df= 63) associated to
Guzmania multiflora, but not more richness of these (richness of adult-larvae t = 0.108,
p= 0.913, df = 63; richness of aquatic-terrestrial t = -0.593, p= 0.555, df = 63).
Regarding the functional groups, the shredders’ group, had mainly by Scirtes sp. and
Chironomidae, showed high abundance in regards to other functional groups, and
richness was high for shredders and predators (ANOVA; abundance: F4, 315= 76.9, p
<2e-16; ANOVA richness F4, 315= 158.4, p <2e-16 (Figure 2.3). Abundance and richness
differed between dispersal types (ANOVA abundance: F2, 186= 64, p <2e-16; ANOVA
richness: F4, 315 = 87.67, p <2e-16, as a greater richness and abundance was found for
aerial active dispersal (Figure 2.3). In addition, habitat complexity affects functional
41 and predator individuals and aerial active dispersion, as well as a greater richness of
terrestrial, adult, and shredder individuals and aerial and terrestrial active dispersion. On
the contrary, the resource (litter amount) present in bromeliads is negatively related to
richness of filter feeders and terrestrial active dispersion (Table 2.2).
2.5. DISCUSION
Habitat complexity and resource availability determines community structure in
bromeliads (Jocque and Field, 2014; Marino et al., 2013; Srivastava, 2006); moreover,
these factors could determine biological traits. Our study sought to determine the
relation between habitat complexity and resource availability and biological traits of
invertebrates associated to Guzmania multiflora. We predicted that bromeliads with
high leaf number and litter amount supported more invertebrate species and abundance,
as well as more abundance and richness of a particular category of biological traits. Our
results showed that habitat complexity not only alters the taxonomical diversity of
invertebrates in bromeliads, but also the functional diversity of invertebrates through
changes in the abundance and richness of biological traits.
2.5.1. Taxonomical diversity
As we expected, arthropods were the most diverse and abundant group in the bromeliad
Guzmania multiflora, with a high abundance of immature stages of Diptera and high
diversity of functional groups such as shredders, filter feeders, and predators (Merrit and
Cummins, 2008; Stehr, 2005). Immature stages of Diptera have special adaptations to
42 oxygen from the air and support the low oxygen concentration. Bibionidae (Mestre et
al., 2001), Anisopodidae (Kitching, 1971), Ceratopogonidae (Atrichopogon sp. and
Stilobezzia sp.), Pychodidae (Pericoma sp.) (Campos et al., 2011; Frank et al., 2004),
Chironomidae (Cranston, 2007; Frank, and Lounibos, 2009), and Culicidae have been
reported in bromeliads and/or treeholes. The latter were the most abundant Diptera
families in Guzmania multiflora. Chironomidae is common in bromeliads, where they
have a high abundance and are relevant in energy flow through the ecosystem (Tokeshi,
1995). Culicidae have been well studied given they are vectors of tropical diseases such
as malaria and yellow fever, and most are filter feeders and browse on small particles,
such as Culex sp. and Wyeomyia sp. (Porter and Wolff, 2004). In Guzmania multiflora,
we found the predator Toxorhynchites sp., which is a common predator in treeholes
(Fincke, 1999; Lounibos et al., 2001) and in the bromeliad Aechmea mertensii in French
Guiana (Céréghino et al., 2011).
On the other hand, some morphospecies are a novel record for bromeliads; for instance,
Dixidae individuals feed on small particles in the water column and little is known
about these species in tropical regions (Wagner et al, 2008). In addition, Systelloderes
sp. (Hemiptera: Enicocephalidae) is a predator that lives on the ground or in places
where organic matter in decomposition is accumulated (Schuh and Slater, 1995), and
has been reported in Vriesea inflata and Tillandsia spp. (Bromeliaceae) of Brazil and
Peru (Mestre et al., 2001; Parker et al., 2012). Finally, Oreiallagma oreas (Odonata:
Coenagrionidae) is the only species of Oreiallagma for which its adult stage was
reported in Colombia (department of Valle del Cauca) at 2300 m.a.s.l. in 1918 (von
Ellenrieder and Garrison, 2008), and the biology and ecology of adults and larvae are
43 Habitat complexity increases richness and abundance of invertebrates in Guzmania
multiflora, given that bromeliads with high leaf number are bigger than bromeliads with
low leaf number. As a consequence, bigger bromeliads have more habitats available to
biota, reducing interspecific and intraspecific competition through providing more niche
space (Cérénghino et al., 2012; Singer et al., 2010), more tanks for retaining more water
and reducing the susceptibility to drought, more canopy litter that is divided among
tanks offering more habitat heterogeneity, and, finally, more adults using the bromeliad
for oviposition (Sota et al., 1994). Litter is a food resource for phytotelmata biota; its
quantity and quality are factors that control population dynamics as well as richness and
abundance of invertebrates (Daugherty and Juliano, 2001). Nevertheless, in our study,
leaf number, rather than litter amount, was a relevant factor on the community, because
fauna chose the tank according to the space available for survivorship and growth of
larvae.
2.5.2. Biological traits diversity
The persistence of species in an ecosystem depends on appropriate morphological,
physiological, and behavioral characteristics that result from species adaptations to
environmental conditions imposed in the ecosystem (Reiss et al., 2009; Paradise, 1998).
For bromeliads, the majority of fauna develops only a part of their life cycle in the
bromeliad; therefore, the immature stage of insects live in the bromeliad by feeding,
moulting, and interacting with other species. Although we found high abundance and
richness of aquatic larvae belonging to the immature stage of Diptera families and
Scirtidae (Scirtes sp.), these were unaffected by habitat complexity and resource
44 bromeliads or discontinuity in water inputs could determine the diversity of aquatic and
immature fauna.
Nevertheless, richness and abundance of terrestrial invertebrates and adult richness was
altered by leaf number, since the oldest leaves of the bromeliad offer semiaquatic and
terrestrial habitats for terrestrial organisms, which use the bromeliad to consume insects
that arrive to colonize, insects that emerge, and detritus. For instance, Dermaptera and
other terrestrial shredder benefit from leaf litter accumulated in dry leaves; for example,
spiders build webs over the bromeliad or wait at the underside of leaves to predate
insects (obs. per.).
Predators had high richness in the bromeliad and their abundance was related with
habitat complexity, as has been found in other studies (Burlakova et al., 2011;
Langellotto and Denno, 2004). Habitat complexity alters the predator-prey relationship
because habitat complexity reduces predation risk (Saha et al., 2009). However, the
interaction between predators is favored in more complex habitats by increasing
predation efficiency (Grabowski et al., 2008).
Moreover, shredders facilitate other organisms inhabiting the bromeliad through
breaking leaf litter; for instance, shredders regulate the FPOM (fine particule organic
matter) concentration for filter feeders (Heard and Richardson, 1995; Paradise and
Kuhn, 1999;). Although these showed high abundance in bromeliads, shredder
abundance was unaffected by habitat complexity and resource availability, similar to
that found by Paradise (2004), with the most abundant shredder family Scirtidae
45 to leaf number; more leaves can accumulate more abundance and diversity of food
resources (litter) that can be used by shredders, reducing the predation risk by
damselflies and other aquatic predators, and reducing competition for food resources
and space(McCann and Rooney, 2009).
Other studies have found an increase in the abundance of other functional groups such
as collectors and scrapers in more complex habitats (Burlakova et al., 2011); however,
in our study, scrapers and filter feeder were unaffected by leaf number. On the contrary,
filter feeders richness was reduced where the bromeliad has more litter; due to the litter
decomposition process alter the water pH, which would regulated the presence of filter
feeder, for instance, high litter amount stimulate the detritivores decomposition
(fragmentation) activity over leaves that lead to facilities the presence of Culex sp. and
Wyeomyia sp. through change in the pH (Paradise, 2000; Torreias et al., 2010);
moreover, litter decomposition increase the organic matter available in the bromeliad,
which is essential resource for filter feeder (Kitching, 2001).
Invertebrate with aerial active dispersion are more abundance give that animals with this
dispersion can select and colonizer a new habitat more efficiently those others.
Moreover, the abundance and richness of insects with aerial active dispersion is affected
by habitat complexity, due to insects with aereal active dispersion select the habitat
where ovopositar according to space available for development of immature stage
(Yanoviak , 1998); then insects with aereal active dispersion would select bromeliads
with more leaf number that would receive more detritus and rainwater as a resource for
the survival and develop of the larvae stage (Gename and Monge-Nájera, 2012).
